Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission.

The development of high-throughput genome sequencing enables accurate measurements of levels of sub-consensus intra-host virus genetic diversity and analysis of the role played by natural selection during cross-species transmission. We analysed the natural and experimental evolution of rabies virus...

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Main Authors: Emilie M Bonnaud, Cécile Troupin, Laurent Dacheux, Edward C Holmes, Elodie Monchatre-Leroy, Marion Tanguy, Christiane Bouchier, Florence Cliquet, Jacques Barrat, Hervé Bourhy
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-06-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1007799
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author Emilie M Bonnaud
Cécile Troupin
Laurent Dacheux
Edward C Holmes
Elodie Monchatre-Leroy
Marion Tanguy
Christiane Bouchier
Florence Cliquet
Jacques Barrat
Hervé Bourhy
author_facet Emilie M Bonnaud
Cécile Troupin
Laurent Dacheux
Edward C Holmes
Elodie Monchatre-Leroy
Marion Tanguy
Christiane Bouchier
Florence Cliquet
Jacques Barrat
Hervé Bourhy
author_sort Emilie M Bonnaud
collection DOAJ
description The development of high-throughput genome sequencing enables accurate measurements of levels of sub-consensus intra-host virus genetic diversity and analysis of the role played by natural selection during cross-species transmission. We analysed the natural and experimental evolution of rabies virus (RABV), an important example of a virus that is able to make multiple host jumps. In particular, we (i) analyzed RABV evolution during experimental host switching with the goal of identifying possible genetic markers of host adaptation, (ii) compared the mutational changes observed during passage with those observed in natura, and (iii) determined whether the colonization of new hosts or tissues requires adaptive evolution in the virus. To address these aims, animal infection models (dog and fox) and primary cell culture models (embryo brain cells of dog and fox) were developed and viral variation was studied in detail through deep genome sequencing. Our analysis revealed a strong unidirectional host evolutionary effect, as dog-adapted rabies virus was able to replicate in fox and fox cells relatively easily, while dogs or neuronal dog cells were not easily susceptible to fox adapted-RABV. This suggests that dog RABV may be able to adapt to some hosts more easily than other host variants, or that when RABV switched from dogs to red foxes it lost its ability to adapt easily to other species. Although no difference in patterns of mutation variation between different host organs was observed, mutations were common following both in vitro and in vivo passage. However, only a small number of these mutations also appeared in natura, suggesting that adaptation during successful cross-species virus transmission is a complex, multifactorial evolutionary process.
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spelling doaj.art-c47eca9c1a1e4683a08d38d84849f8ea2022-12-21T22:36:57ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742019-06-01156e100779910.1371/journal.ppat.1007799Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission.Emilie M BonnaudCécile TroupinLaurent DacheuxEdward C HolmesElodie Monchatre-LeroyMarion TanguyChristiane BouchierFlorence CliquetJacques BarratHervé BourhyThe development of high-throughput genome sequencing enables accurate measurements of levels of sub-consensus intra-host virus genetic diversity and analysis of the role played by natural selection during cross-species transmission. We analysed the natural and experimental evolution of rabies virus (RABV), an important example of a virus that is able to make multiple host jumps. In particular, we (i) analyzed RABV evolution during experimental host switching with the goal of identifying possible genetic markers of host adaptation, (ii) compared the mutational changes observed during passage with those observed in natura, and (iii) determined whether the colonization of new hosts or tissues requires adaptive evolution in the virus. To address these aims, animal infection models (dog and fox) and primary cell culture models (embryo brain cells of dog and fox) were developed and viral variation was studied in detail through deep genome sequencing. Our analysis revealed a strong unidirectional host evolutionary effect, as dog-adapted rabies virus was able to replicate in fox and fox cells relatively easily, while dogs or neuronal dog cells were not easily susceptible to fox adapted-RABV. This suggests that dog RABV may be able to adapt to some hosts more easily than other host variants, or that when RABV switched from dogs to red foxes it lost its ability to adapt easily to other species. Although no difference in patterns of mutation variation between different host organs was observed, mutations were common following both in vitro and in vivo passage. However, only a small number of these mutations also appeared in natura, suggesting that adaptation during successful cross-species virus transmission is a complex, multifactorial evolutionary process.https://doi.org/10.1371/journal.ppat.1007799
spellingShingle Emilie M Bonnaud
Cécile Troupin
Laurent Dacheux
Edward C Holmes
Elodie Monchatre-Leroy
Marion Tanguy
Christiane Bouchier
Florence Cliquet
Jacques Barrat
Hervé Bourhy
Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission.
PLoS Pathogens
title Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission.
title_full Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission.
title_fullStr Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission.
title_full_unstemmed Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission.
title_short Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission.
title_sort comparison of intra and inter host genetic diversity in rabies virus during experimental cross species transmission
url https://doi.org/10.1371/journal.ppat.1007799
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